ORIGINAL ARTICLE pISSN 1598-9100 • eISSN 2288-1956 https://doi.org/10.5217/ir.2020.00009 Intest Res 2021;19(2):239-246 Postgastrectomy gastric cancer patients are at high risk for colorectal neoplasia: a case control study

Tae-Geun Gweon1*, Kyu-Tae Yoon1*, Chang Hyun Kim2, Jin-Jo Kim2 1Division of , Department of Internal Medicine and 2Department of Surgery, College of Medicine, The Catholic University of Korea, Seoul, Korea

Background/Aims: Several studies have shown that colorectal (CRN) including (CRC) may be prevalent in patients with gastric cancer. However, in most of these studies, to investigate the prevalence of CRN was performed prior to surgery. We aimed to investigate whether CRN was more prevalent in postgastrectomy gastric cancer patients than in healthy individuals. Methods: We reviewed the medical records of those patients within a cohort of gastric can- cer patients with gastrectomy who underwent colonoscopy between 2016 and 2017. Controls age- and sex-matched with gas- tric cancer patients at a 2:1 ratio were identified among those who underwent colonoscopy at a health-promotion center. The frequencies of CRN, advanced CRN (ACRN), and CRC among patients with gastrectomy were compared with those in the con- trol subjects. A total of 744 individuals (gastric cancer, 248; control, 496) were included. Results: The rates of CRN and ACRN in the gastric cancer group were higher than those in the healthy individuals (CRN, 47.6% vs. 34.7%, P<0.001; ACRN, 16.9% vs. 10.9%, P=0.020). The rate of CRC was comparable between the 2 groups (2.0% vs. 0.6%,P =0.125). Multivariate analysis identi- fied previous gastrectomy for gastric cancer and male sex as significant risk factors for (A)CRN. Conclusions: CRN and ACRN were more prevalent in patients who underwent surgery for gastric cancer than in the control group. Regular surveillance colo- noscopy at appropriate intervals is indicated after gastrectomy. (Intest Res 2021;19:239-246)

Key Words: neoplasms; Colonoscopy; Colorectal ; Colonoscopic surveillance

INTRODUCTION doscopic treatment in gastric cancer patients was reported as 1%–4%.3-6 Although the prevalence of colorectal neoplasms The prognosis of patients with gastric cancer has improved (CRN) including CRC was higher in patients with gastric can- with detection at early stages and advances in treatment mo- cer than in healthy individuals, most studies have investigated dalities.1,2 Therefore, detection of secondary cancer is as im- the prevalence of concomitant CRN at the time of surgical re- portant as surveillance of gastric cancer recurrence. Colorec- section or endoscopic resection of gastric cancer. CRC devel- tal cancer (CRC) has been recognized as the most common ops from benign CRN through the -carcinoma se- synchronous in patients with gastric cancer.3-5 The quence.7 Regular surveillance colonoscopy based on the num- prevalence of concomitant CRC at the time of surgical or en- ber and histology of resected CRN is recommended after re- section of CRN.8,9 No previous study has investigated the prev- Received March 9, 2020. Revised May 21, 2020. Accepted June 3, 2020. alence of CRN after surgical treatment of gastric cancer. In this Correspondence to Chang Hyun Kim, Department of Surgery, Incheon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 56 study, we aimed to investigate whether CRN was more preva- Dongsu-ro, Bupyeong-gu, Incheon 21431, Korea. Tel: +82-32-280-5052, lent in gastric cancer patients after surgical treatment than in Fax: +82-32-280-5987, E-mail: [email protected] healthy individuals. *These authors contributed equally to this study. This study was presented as an oral poster at IMKASID on April 13-14, 2018, in Seoul, Korea.

© Copyright 2021. Korean Association for the Study of Intestinal Diseases. All rights reserved. 239 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Silvio Danese, et al. • iSTART consensus recommendations

Tae-Geun Gweon, et al. • Colonoscopy after gastrectomy

METHODS plastic lesions (hyperplastic, lymphoid, inflammatory). Ad- vanced CRN (ACRN) was defined when one of the following Among a cohort of gastric patients who un- criteria was met: (1) adenocarcinoma; (2) adenoma sized at derwent gastrectomy at Incheon St. Mary’s Hospital (Incheon, least 1 cm; (3) the presence of at least 3 ; and (4) the Republic of Korea), we reviewed the medical records of con- presence of villous adenoma or high-grade .8,20 The secutive subjects who underwent colonoscopy between Janu- rate of CRN, ACRN, and CRC and the number of adenomas ary 2016 and December 2017.10 We excluded patients with ce- per patient were analyzed. The protocol of this study was ap- cal intubation failure; or inadequate bowel preparation. Colo- proved by the Institutional Review Board of Incheon St. Mary’s noscopy was performed at least 1 year after gastrectomy. In Hospital (IRB No. OC17MES0031). Written informed consent our center, colonoscopy for gastric cancer patients is included was obtained from all patients. in the routine staging work-up before surgery.11 Therefore, most gastric cancer patients undergo colonoscopy before surgery. 3. Statistical Analysis The control group comprised healthy subjects who underwent All statistical analyses were performed using IBM SPSS ver- colonoscopy at the health-care center of our institution during sion 20 (IBM Corp., Armonk, NY, USA). Continuous variables the study period and were matched with gastric cancer patients were compared using Student t-test or the Mann-Whitney test by age and sex in a 2:1 ratio. Demographic characteristics, bow- when appropriate. Categorical variables are presented as el preparation quality, and results of colonoscopy were inves- number (percent) and compared using the chi-square or Fish- tigated. Cancer staging and type of surgery were investigated er exact tests. We compared the clinical data and prevalence in the gastric cancer group. Cancer staging was performed at of (A)CRN and CRC between the gastric cancer and the con- the time of gastrectomy using the 7th edition of the American trol group. To investigate the factors contributing to having (A) Joint Committee on Cancer Staging Manual.12 CRN or CRC, we compared the clinical data of all the patients with and without (A)CRN or CRC. Logistic regression model- 1. Colonoscopic Examinations ing was used to perform multivariate analysis of risk factors Colonoscopy was performed by 3 attending physicians with for (A)CRN or CRC that were found to be significant in the uni- more than 4 years of experience using an Olympus (Olympus, variate analysis. Odds ratio (OR) and 95% confidence interval Seoul, Korea) series Q260 or Q290 colonoscope.13,14 Bowel (CI) were calculated for the prevalence of (A)CRN and CRC. preparation was done with 4 L of polyethylene glycol. To ob- A P-value <0.05 was considered significant. tain optimal bowel cleansing, patients were instructed to in- gest additional liquid until no solid particles were observed in RESULTS the bowel effluent.15 Bowel cleansing quality was assessed us- ing the Aronchick scale.16,17 resection was performed Two hundred and sixty-six patients with gastric cancer under- during withdrawal of the colonoscope. The colonoscopists went colonoscopy during the study period. Of these patients, were encouraged to observe the colonic mucosa for at least 6 18 were excluded because of cecal intubation failure (n=5) or minutes.18 Polyp resection was performed by cold snare pol- inadequate bowel preparation (n=13). After matching of heal­ ypectomy or conventional endoscopic mucosal resection at thy subjects, a total of 744 patients were finally included in this the physician’s discretion. Histologic assessment of resected study: gastric cancer (n=248) and healthy control (n=496). polyps was performed by specialist gastrointestinal patholo- The demographic and clinical data of the 2 groups are shown gists. Cecal intubation time, colonoscope withdrawal time, and in Table 1. Age, sex, comorbidities, family history of CRC, and total colonoscopy time were analyzed. Colonoscope withdraw- factors related to previous colonoscopy were similar between al time was determined as the time difference between photo- the 2 groups. Body mass index was lower in the patients with graphic documentation of the cecum and anus in patients gastrectomy (gastric cancer group 21.3 kg/m2 vs. control group who did not undergo any procedures such as a biopsy or pol- 24.4 kg/m2, P<0.001). Indications for colonoscopy differed be- ypectomy.19 tween the 2 groups (P<0.001). The median interval between surgery and colonoscopy in the gastric cancer group was 51 2. Definition months. CRN included adenomas or cancers but excluded nonneo-

240 www.irjournal.org •

https://doi.org/10.5217/ir.2020.00009 • Intest Res 2021;19(2):239-246

Table 1. Baseline Characteristics Characteristics Gastric cancer (n=248) Control (n=496) P-value Age (yr) 62.4±8.5 62.4±8.5 1.000 Male sex 148 (60.0) 296 (60.0) 1.000 Body mass index (kg/m2) 21.3±2.2 24.4±3.2 <0.001 Comorbidity Diabetes 47 (19.0) 105 (20.2) 0.479 Hypertension 55 (22.2) 92 (18.5) 0.241 15 (6.0) 25 (5.0) 0.566 Family history of colorectal cancer 16 (6.6) 26 (5.2) 0.467 Factors of previous colonoscopy Previous history of colonoscopy 225 (90.7) 433 (87.3) 0.168 Previous removal of colorectal polyp 100 (40.3) 186 (37.5) 0.456 Interval of previous colonoscopy (yr)a 3 (3–4) 3 (2–3) 0.490 Indication of colonoscopy <0.001 Screening 117 (47.2) 213 (42.9) Surveillance 120 (48.4) 202 (40.7) Others 11 (4.4) 81 (16.3) Type of gastrectomy Total gastrectomy 45 (18.1) NA Subtotal gastrectomy 203 (81.9) NA Laparoscopic surgery 158 (63.7) NA Cancer stageb I 164 (66.1) NA II 48 (19.4) NA III 36 (14.5) NA Interval between surgery and colonoscopy (mon) 51 (23–58) NA Values are presented as mean±standard deviation, number (%), or median (interquartile range). aData were obtained in patients with history of colonoscopy. bCancer staging was done according to American Joint Committee on Cancer 7th edition.16 NA, not applicable.

1. Prevalence of CRN cancer was found in 3 gastric cancer patients (Fig. 2). In the The rate of polyp detection in the gastric cancer group was gastric cancer group, the rate of CRN (stage I 48.8% vs. stage 55.6%, which was higher than that in the control group (46.4%, II+III 45.2%, P =0.597), ACRN (stage I 15.2% vs. stage II+III P =0.017). The prevalence of CRN and ACRN in the gastric 20.2%, P=0.321) and CRC (stage I 1.2% vs. stage II+III 3.6%, cancer group was higher than that in the control group (CRN: P=0.340) was not higher in the advanced cancer stage. How- 47.6% vs. 34.7%, OR, 1.710; 95% CI, 1.254–2.332; P<0.001 and ever, all metastatic cancer was found in gastric cancer with ACRN: 16.9% vs. 10.9%, OR, 1.669; 95% CI, 1.079–2.580; P=0.020) stage III. (Table 2, Fig. 1). However, the rate of CRC was comparable be- tween the 2 groups (gastric cancer 2% vs. control 0.6%, P=0.125). 2. Results of Colonoscopy The rate of sessile serrated adenoma/polyp was comparable The details of colonoscopy are shown in Table 2. The time between the 2 groups (2.4% vs. 2.0%, P=0.721). The mean num- needed for colonoscope insertion was longer in the gastric ber of adenomas per patient was comparable between the 2 cancer group than in the control group (gastric cancer 5.0 groups (gastric cancer 0.9 vs. control 0.7, P=0.833). Metastatic minutes vs. control 3.9 minutes, P<0.001). Withdrawal time www.irjournal.org 241 Silvio Danese, et al. • iSTART consensus recommendations

Tae-Geun Gweon, et al. • Colonoscopy after gastrectomy

was comparable for both groups (gastric cancer 6.8 minutes ing efficacy in the control group was superior to that in the -pa vs. control 6.7 minutes, P=0.386). Total colonoscopy time was tients with gastrectomy (P<0.001). Perforation or postpolyp- longer in the gastric cancer patients (gastric cancer 16.8 min- ectomy bleeding did not occur in either group. utes vs. control 14.1 minutes, P<0.001). Overall bowel cleans- 3. Risk Factors for CRN Table 2. Results of Colonoscopy Male sex and a history of gastrectomy were significant risk fac- tors for CRN in univariate analysis (Table 3). The patients with Gastric Control Characteristics cancer P-value CRN were older than those without CRN (CRN 63.2 years vs. (n=496) (n=248) without CRN 61.9 years, P=0.042). Multivariate analysis re- Colorectal neoplasm vealed that male sex (OR, 2.183; 95% CI, 1.590–2.996) and a All colorectal neoplasm 118 (47.6) 172 (34.7) <0.001 history of surgery for gastric cancer (OR, 1.748; 95% CI, 1.274– Advanced colorectal neoplasm 42 (16.9) 54 (10.9) 0.020

No. of adenoma ≥3 30 (12.1) 32 (6.5) 0.009 60 P<0.001 Size of adenoma ≥1 cm 15 (6.0) 22 (4.4) 0.034 50 47.6 Villous or high-grade dysplasia 13 (5.2) 25 (5.0) 0.906 Colorectal cancer 5 (2.0) 3 (0.6) 0.125 40 34.7 Sessile serrated adenoma/polyp 6 (2.4) 10 (2.0) 0.721 30 P=0.020

Time related to colonoscopy (min) Rate (%) Insertion time 5.0±2.7 3.9±2.6 <0.001 20 16.9 Withdrawal timea 6.8±1.3 6.7±1.5 0.386 10.9 P=0.125 10 Total procedure time 16.8±3.4 14.1±2.7 <0.001 2.0 0.6 Bowel cleansing <0.001 0 Neoplasm Advanced neoplasm Cancer Excellent 34 (13.7) 166 (33.5) Gastric cancer n=118 n=42 n=5 Good 112 (45.2) 217 (43.8) Control n=172 n=54 n=3 Fair 102 (41.1) 113 (22.8) Fig. 1. Comparison of the rate of detection of colorectal neoplasm Values are presented as number (%) or mean±standard deviation. in the 2 groups. The rates of colorectal neoplasm and advanced aWithdrawal time was checked in 110 in the gastric cancer group and 266 colorectal neoplasm were significantly higher in the gastric can- in the control group. cer group than in the control group.

A B

Fig. 2. Detection of metastatic gastric cancer. (A) A luminal obstructing mass was noted during colonoscopy. (B) Positron emission to- mography-computed tomography revealed prominent fluorodeoxyglucose uptake at the ascending colon.

242 www.irjournal.org •

https://doi.org/10.5217/ir.2020.00009 • Intest Res 2021;19(2):239-246

Table 3. Risk Factors of Colorectal Neoplasm of All Study Subjects

Colorectal neoplasm Absent Multivariate analysis Characteristics P-value (n=290) (n=454) OR 95% CI P-value Age (yr) 63.2±8.0 61.9±8.7 0.042 0.983 0.965–1.001 0.057 Male sex 205 (70.7) 239 (52.6) <0.001 2.183 1.590–2.996 <0.001 Body mass index (kg/m2) 23.5±3.2 23.4±3.3 0.621 Diabetes 60 (20.7) 92 (20.3) 0.888 Family history of colorectal cancer 20 (6.9) 22 (4.8) 0.237 History of colorectal polyp 100 (34.5) 186 (41.0) 0.076 Gastric cancer 118 (40.7) 130 (28.6) <0.001 1.748 1.274–2.400 0.001 Values are presented as mean±standard deviation or number (%). OR, odds ratio; CI, confidence interval.

Table 4. Risk Factors of Advanced Colorectal Neoplasm of All Study Subjects

Advanced colorectal Absent Multivariate analysis Characteristics P-value neoplasm (n=96) (n=648) OR 95% CI P-value Age (yr) 63.1±8.5 62.3±8.5 0.375 Male sex 79 (82.3) 365 (56.3) <0.001 3.620 2.092–6.265 <0.001 Body mass index (kg/m2) 23.1±3.0 23.5±3.3 0.316 Diabetes 25 (26.0) 127 (19.6) 0.144 Family history of colorectal cancer 8 (8.3) 34 (5.2) 0.215 History of colorectal polyp 32 (33.3) 256 (39.5) 0.247 Gastric cancer 42 (43.8) 206 (31.8) <0.001 1.705 1.094–2.659 0.019 Values are presented as mean±standard deviation or number (%). OR, odds ratio; CI, confidence interval.

2.400) were significant risk factors for CRN. A comparison of has been reported to be inversely proportional to the con- individuals with and without ACRN is shown in Table 4. Uni- sumption of nonsteroidal anti-inflammatory drugs (NSAIDs) variate analysis revealed that male sex and a history of gastric and aspirin.22 Our group previously investigated the useful- cancer were significant risk factors for ACRN. After multivari- ness of screening colonoscopy in gastric cancer patients be- ate analysis, male sex (OR, 3.620; 95% CI, 2.092–6.265) and a fore surgery,11 and showed that CRN, ACRN, and CRC were history of surgery for gastric cancer (OR, 1.705; 95% CI, 1.094– more prevalent in the gastric cancer group than in healthy 2.659) were identified as significant risk factors. There was no controls. Although CRC is the most common synchronous significant difference between patients with and without CRC. cancer with gastric cancer, the relationship between these 2 cancers has not been determined. Several studies have sug- DISCUSSION gested that , a causative organism of gastric cancer, is also a risk factor for CRC.23,24 In the current study, we To our knowledge, this study is the first to investigate the use- compared the prevalence of CRN, ACRN, and CRC between fulness of colonoscopy in gastric cancer patients after gastrec- postgastrectomy gastric cancer patients and healthy individu- tomy. This study confirmed that CRN and ACRN were more als. The prevalence of CRC was numerically higher in the gas- prevalent in patients with gastric cancer after gastrectomy than tric cancer patients than in the control group, but this differ- in healthy individuals. ence was not significant. The prevalence of CRN and ACRN Known risk factors for CRC are diabetes, hyperlipidemia, al- was significantly higher in the gastric cancer group than in the cohol use, and a diet rich in animal fat.21,22 The incidence of CRC healthy controls. In the multivariate analysis, gastric cancer www.irjournal.org 243 Silvio Danese, et al. • iSTART consensus recommendations

Tae-Geun Gweon, et al. • Colonoscopy after gastrectomy

was an independent risk factor for CRN and ACRN. This indi- fined as the amount of time that did not result in any positive cates that regular scheduled colonoscopy should be performed finding that required additional procedures.19,29 In the current after gastrectomy. study, colonoscope withdrawal time was comparable between In the current study we excluded patients who underwent the 2 groups. The rate of adenoma detection has been report- endoscopic resection. In a previous study, the prevalence of ed to be influenced by withdrawal time, which is an important CRN at the time of resection did not differ between the pa- indicator of adequate colonoscopy.27 tients who underwent surgical resection and endoscopic re- We acknowledge several limitations of the current study. First, section.11 Colonoscopy in patients who underwent gastrecto- because of its retrospective design, several patients had missing my is technically demanding because of bowel adhesion. In data. Colonoscope withdrawal time was measured in only 50% our center, colonoscopy before gastrectomy and follow up of the patients. However, colonoscopy for both groups was per- colonoscopy after surgery was usually performed by fellows formed by the same colonoscopists and withdrawal time was (gastroenterologist and surgeon). However, in the current similar for both groups. The use of medications such as aspirin study, the colonoscopy in both groups was performed by same or NSAIDs, which are known to have a protective effect against experience colonoscopists (professor of gastroenterology) CRC development, was not analyzed. Second, the control sub- who are low risk for missing adenoma or having chance of in- jects were matched from those who underwent colonoscopy at terval cancer. a health-promotion center, who were relatively healthy and had Guidelines recommend an initial screening test for CRC in a strong interest in health screening. Indications for colonosco- the general population, starting at age 50, using a stool-based py and bowel cleansing quality differed between the 2 groups. A test or including colonoscopy and sigmoidosco- previous history of abdominal surgery is a risk factor for subop- py.18 Colonoscopy is recognized as the best diagnostic meth- timal bowel cleansing.30 However, we excluded patients with in- od for detecting CRC and has several benefits. First, as well as adequate bowel cleansing and therefore believe that these pa- detecting CRC, colonoscopy can simultaneously treat a pre- rameters did not affect the main outcome of our study. Third, cancerous CRN at the time of diagnosis and hence can pre- this study was not designed to investigate the rate of CRN in the vent CRC.25 Most CRNs found at colonoscopy are less than 1 gastric cancer group and the control group. cm in diameter, and are suitable for conventional methods of Despite the limitations described above, our study has sev- polypectomy including hot or cold snare polypectomy.26,27 Sec- eral strengths. First, using a well-preserved cohort of surgical ond, colonoscopy can detect metastatic cancer after gastrec- data, we included consecutive gastric cancer patients who un- tomy. We identified metastatic cancer in 3 patients in the gas- derwent colonoscopic examination during the study period. tric cancer group. Second, colonoscopic examination was performed by experi- We also compared colonoscopy quality measures between enced endoscopists and quality measures for colonoscopy the 2 groups. The colonoscope insertion time was longer in were met. The rate of adenoma detection was more than 25% the patients who underwent gastrectomy. Colonoscope inser- and colonoscope withdrawal time was longer than 6 minutes tion time is an important technical measure of colonoscopy.28 for both groups. Although the technical difficulty of colonoscope insertion was In conclusion, our study demonstrated that CRN and ACRN not recorded by the colonoscopists, the longer insertion time were more prevalent in postgastrectomy gastric cancer pa- in the gastric cancer group indirectly suggests that colonoscope tients than in healthy individuals. A history of surgery for gas- insertion was more technically demanding in postgastrecto- tric cancer was an independent risk factor for CRN and ACRN. my patients than in the healthy population. We investigated The results of the current study address the importance of reg- colonoscope withdrawal time only in patients who did not ular surveillance colonoscopy after gastrectomy at appropri- undergo any additional procedures such as a biopsy or polyp- ate intervals. Future clinical trials are needed to validate the ectomy. Colonoscope withdrawal time is usually defined as results of this study. the mucosal inspection time excluding time for fluid suction or additional procedures. Thus, it was challenging to analyze ADDITIONAL INFORMATION colonoscope withdrawal time accurately in patients who un- derwent polypectomy or a biopsy. In previous studies, the mean Funding Source inspection time for upper endoscopy or colonoscopy was de- The authors received no financial support for the research,

244 www.irjournal.org •

https://doi.org/10.5217/ir.2020.00009 • Intest Res 2021;19(2):239-246 authorship, and/or publication of this article. 7. Leslie A, Carey FA, Pratt NR, Steele RJ. The colorectal adeno- ma-carcinoma sequence. Br J Surg 2002;89:845-860. Conflict of Interest 8. Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson No potential conflict of interest relevant to this article was DA, Levin TR. Guidelines for colonoscopy surveillance after reported. screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenter- Author Contribution ology 2012;143:844-857. Conceptualization: Gweon TG. Data curation: Yoon KT. For- 9. Choi WS, Han DS, Eun CS, et al. Three-year colonoscopy sur- mal analysis: Yoon KT. Investigation: Yoon KT. Methodology: veillance after polypectomy in Korea: a Korean Association Gweon TG, Yoon KT, Kim JJ. Project administration: Gweon for the Study of Intestinal Diseases (KASID) multicenter pro- TG. Software: Yoon KT. Supervision: Kim CH. Validation: Kim spective study. Intest Res 2018;16:126-133. JJ. Writing - original draft: Gweon TG, Yoon KT. Writing - re- 10. Gweon TG, Huh CW, Ji JS, Kim CH, Kim JJ, Park SM. Compari- view & editing: Kim JJ. Approval of final manuscript: all authors. son of bowel-cleansing efficacy of split-dose and same-day dose bowel preparation for afternoon colonoscopy in patients Others with gastrectomy: a prospective randomized study. Surg En- We gratefully thank Ha Soon Kang and Fr. Youn Hui Kang dosc 2020;34:4413-4421. Thomas Aquinas. 11. Yoo HM, Gweon TG, Seo HS, et al. Role of preoperative colo- noscopy in patients with gastric cancer: a case control study ORCID of the prevalence of coexisting colorectal neoplasms. Ann Gweon TG https://orcid.org/0000-0002-0884-7228 Surg Oncol 2013;20:1614-1622. Yoon KT https://orcid.org/0000-0001-9219-9624 12. Washington K. 7th Edition of the AJCC cancer staging manu- Kim CH https://orcid.org/0000-0003-1567-4318 al: stomach. Ann Surg Oncol 2010;17:3077-3079. Kim JJ https://orcid.org/0000-0003-1011-8793 13. Huh CW, Gweon TG, Seo M, Ji JS, Kim BW, Choi H. Validation of same-day bowel preparation regimen using 4L polyethyl- REFERENCES ene glycol: comparison of morning and afternoon colonosco- py. Medicine (Baltimore) 2018;97:e12431. 1. Jun JK, Choi KS, Lee HY, et al. Effectiveness of the Korean Na- 14. Seo M, Gweon TG, Huh CW, Ji JS, Choi H. Comparison of tional Program in reducing gastric cancer bowel cleansing efficacy, safety, bowel movement kinetics, mortality. Gastroenterology 2017;152:1319-1328. and patient tolerability of same-day and split-dose bowel 2. Allemani C, Matsuda T, Di Carlo V, et al. Global surveillance of preparation using 4 L of polyethylene glycol: a prospective trends in cancer survival 2000-14 (CONCORD-3): analysis of randomized study. Dis Colon 2019;62:1518-1527. individual records for 37 513 025 patients diagnosed with one 15. Lee HS, Byeon JS. Bowel preparation, the first step for a good of 18 cancers from 322 population-based registries in 71 coun- quality colonoscopy. Intest Res 2014;12:1-2. tries. Lancet 2018;391:1023-1075. 16. Aronchick CA, Lipshutz WH, Wright SH, Dufrayne F, Berg- 3. Ikeda Y, Saku M, Kawanaka H, Nonaka M, Yoshida K. Features man G. A novel tableted purgative for colonoscopic prepara- of second primary cancer in patients with gastric cancer. On- tion: efficacy and safety comparisons with Colyte and Fleet cology 2003;65:113-117. Phospho-Soda. Gastrointest Endosc 2000;52:346-352. 4. Lee JH, Bae JS, Ryu KW, et al. Gastric cancer patients at high- 17. Gweon TG, Kim SW, Noh YS, et al. Prospective, randomized risk of having synchronous cancer. World J Gastroenterol 2006; comparison of same-day dose of 2 different bowel cleanser 12:2588-2592. for afternoon colonoscopy: picosulfate, magnesium oxide, 5. Eom BW, Lee HJ, Yoo MW, et al. Synchronous and metachro- and citric acid versus polyethylene glycol. Medicine (Balti- nous cancers in patients with gastric cancer. J Surg Oncol 2008; more) 2015;94:e628. 98:106-110. 18. European Colorectal Cancer Screening Guidelines Working 6. Saito S, Hosoya Y, Togashi K, et al. Prevalence of synchronous Group, von Karsa L, Patnick J, et al. European guidelines for colorectal neoplasms detected by colonoscopy in patients quality assurance in colorectal cancer screening and diagno- with gastric cancer. Surg Today 2008;38:20-25. sis: overview and introduction to the full supplement publica-

www.irjournal.org 245 Silvio Danese, et al. • iSTART consensus recommendations

Tae-Geun Gweon, et al. • Colonoscopy after gastrectomy

tion. Endoscopy 2013;45:51-59. fecal immunochemical testing in colorectal-cancer screening. 19. Barclay RL, Vicari JJ, Doughty AS, Johanson JF, Greenlaw RL. N Engl J Med 2012;366:697-706. Colonoscopic withdrawal times and adenoma detection dur- 26. Papastergiou V, Paraskeva KD, Fragaki M, et al. Cold versus ing screening colonoscopy. N Engl J Med 2006;355:2533-2541. hot endoscopic mucosal resection for nonpedunculated color­ 20. Kim SY, Kim TI. Serrated neoplasia pathway as an alternative ectal polyps sized 6-10 mm: a randomized trial. Endoscopy route of colorectal cancer carcinogenesis. Intest Res 2018;16: 2018;50:403-411. 358-365. 27. Regula J, Rupinski M, Kraszewska E, et al. Colonoscopy in color­ 21. Ferrari P, Jenab M, Norat T, et al. Lifetime and baseline alcohol ectal-cancer screening for detection of advanced neoplasia. N intake and risk of colon and rectal cancers in the European Engl J Med 2006;355:1863-1872. prospective investigation into cancer and nutrition (EPIC). 28. Jaruvongvanich V, Sempokuya T, Laoveeravat P, Ungprasert P. Int J Cancer 2007;121:2065-2072. Risk factors associated with longer cecal intubation time: a 22. Chan AT, Giovannucci EL. Primary prevention of colorectal systematic review and meta-analysis. Int J Colorectal Dis 2018; cancer. Gastroenterology 2010;138:2029-2043. 33:359-365. 23. Lee YC, Chiang TH, Chou CK, et al. Association between He- 29. Park JM, Huo SM, Lee HH, Lee BI, Song HJ, Choi MG. Longer licobacter pylori eradication and gastric cancer incidence: a observation time increases proportion of neoplasms detected systematic review and meta-analysis. Gastroenterology 2016; by esophagogastroduodenoscopy. Gastroenterology 2017; 150:1113-1124. 153:460-469. 24. Zumkeller N, Brenner H, Zwahlen M, Rothenbacher D. Heli- 30. Woo DH, Kim KO, Jeong DE, et al. Prospective analysis of fac- cobacter pylori infection and colorectal cancer risk: a meta- tors associated with inadequate bowel preparation for colo- analysis. Helicobacter 2006;11:75-80. noscopy in actual clinical practice. Intest Res 2018;16:293-298. 25. Quintero E, Castells A, Bujanda L, et al. Colonoscopy versus

246 www.irjournal.org